Dairy farmer meets Alien: The braconid wasp Lysiphlebus fabarum harvests honeydew from aphids before literally stabbing them in the back so their offspring can develop inside of the aphids’ bodies.
There are many unlikely relationships in the animal kingdom. Personally, I’m a fan of “Bonedigger” the lion and “Milo” the dachshund, but there are some pretty odd couples in the insect world as well. I recently stumbled across a research piece studying the behavior of a parasitoid wasp that attacks black bean aphids. Interestingly enough, the wasps mimic ant behavior to effectively “coax” the aphids into a false sense of security before stabbing them with their sharp ovipositor and inserting their eggs, which hatch to feed on the aphids from the inside out. Remarkably, these behaviors involve some degree of cooperation from the aphid, and when ants are present, there’s potential for some unlikely mutualism among all three species (although, admittedly, not so much between the aphids and wasps).
Lysiphlebus fabarum forages in ant-tended black bean aphid (Aphis fabae) colonies. Primarily, the aphid is the unfortunate host to developing L. fabarum larvae. In addition, adult wasps feed on aphid honeydew secretions, which is similar to host feeding in other parasitoid–host systems. But unlike host feeding, honeydew feeding does not harm the aphids, instead requiring host cooperation.
Female L. fabarum wasps promote honeydew secretion by mimicking the anntenal drumming of ants, and employ similar antennal movements while probing potential hosts prior to oviposition. Switching between the roles of ant mimic and parasitoid overall reduce the defensive responses of aphids: kicking, thrashing, dispersing, and secreting a waxy, glue-like substance from their cornicles (these cornicle secretions can fuse mandibles, antennae, legs, etc., leading to the death of the wasp).
Lysiphlebus spp. also possess cuticular hydrocarbons and lipids that identify them as aphids to help mask their presence from ants. Apparently their chemical camouflage is so good that it can be difficult for wasps to identify their conspecifics. This camouflage is an evolutionary response to ant aggression, since ants ferociously protect the aphids they tend to. And for L. fabarum, mimicry of ant behavior provides additional protection—not because the ants themselves are fooled, but because it makes aphids more inclined to secrete honeydew in the future.
So a few aphids are lost to parasitism, but the others are more productive—a benefit for hungry wasps as well as ants. In turn, ants offer protection for wasp offspring, albeit unintentionally. Ultimately there is potential for mutualism between ants and L. fabarum, as long as the wasps continue to parasitize only a small fraction of the aphid population. Of course, none of this could have happened if the parasitoid wasps didn’t take advantage of the already-existing mutualism between ants and aphids.
Rasekh A, Michaud JP, Kharazi-Pakdel A, & Allahyari H. (2010). Ant mimicry by an aphid parasitoid, Lysiphlebus fabarum. Journal of Insect Science, 10(1). doi:10.1673/031.010.12601
Microcephaly. Neurological disorders. Guillain-Barré. Described by the World Health Organization as a “Public Health Emergency of International Concern.”
…and up to 80% of adults are asymptomatic.
The Zika virus carries with it some pretty nasty health complications. It is mosquito-borne, although sexual transmission has been documented, which carries unknown epidemiological implications. In the United States, there are two mosquitoes capable of transmitting Zika virus: Aedes aegypti and Aedes albopictus.
Ae. albopictus, that cute little guy pictured below, can be found as far north as Minnesota. Which, according to the media, means: Expect Zika in Minnesota! It’s coming! Run!
But before you read any further, let me assure you—it’s unlikely Zika will become endemic to the northern US. There may be the possibility of transmission by mosquitoes, but there are many factors that will limit the spread of the virus to mosquito populations in temperate climates.
These maps from the CDC (below) show the ranges of Ae. aegypti and Ae. albopictus in the United States. Although both species are capable of transmitting Zika virus, Ae. aegypti is a better vector than Ae. albopictus (even better news for Minnesotans!). Yet there have been zero cases of Zika in the US (to date) that were locally acquired (from our own mosquitoes).
Let’s zoom out from the U.S. for a minute. Here is a map from the newsletter In Homeland Security, which shows the global distribution of Ae. aegypti:
Okay, so this is essentially where we can expect the mosquito to live. But where does Zika live? Can it be found wherever the mosquito is found?
Many researchers and health organizations have analogized Zika virus to dengue, which is a health risk wherever Ae. aegypti is found. Since dengue and Zika both share mosquito vectors, have similar pathology, and origins near the tropics, we use what we know about dengue to create epidemiological models for Zika.
But can we actually do that, using dengue by proxy?
As the image suggests, dengue virus has a complex ecology than can’t simply be defined by the distribution of its arthropod vector. There are biological, environmental, climatic, and cultural restraints that keep dengue more “in check” in some areas rather than others—and we can expect some kind of ecological limitations for Zika virus as well.
Okay, so what restricts the range of a mosquito-borne virus besides, well, the mosquito? Limitations include the exact type of cell receptors required to promote infection in the mosquito midgut, the availability of alternate hosts (which may amplify the viral population), and large scale climatic variations that not only affect a vector population, but also affect viral activity and viral population dynamics.
And what does this mean for Zika in Minnesota? Well, not to spoil the surprise for anyone, but we shouldn’t expect Zika to become established as a mosquito–borne illness in temperate Minnesota. The virus will likely remain confined to the tropics. Our mosquito, Aedes albopictus, is just not as good a vector as Ae. aegypti. While most of the ecology of Zika is unknown, a huge limiting factor for a Minnesota mosquito-borne endemic stems from the temperate climate, unlikely persistence of the virus during the winter, and absence of known alternative hosts (for amplifying the viral population) or of seasonal reintroduction (e.g. migratory birds).
How To Lose a Virus in 10 Days: Defining a Niche for Insect-Borne Pathogens
I am a fan of G. Evelyn Hutchinson’s 1957 description of an ecological niche as an n-dimensional hypervolume. I could devote an entire blog to niche concepts (actually I think I will), but for now consider this basic description: an organism’s niche consists of the abiotic and biotic factors needed for it to survive—stuff like nitrogen, temperature, moisture. For viruses (whether we consider them “alive” or not), their mosquito vector describes only one dimension of their ecology.
The intra-cellular environment. A virus needs to make it way to a particular region of the cell to reproduce. The correct cellular machinery must be present to replicate DNA, build viral proteins, and export the virus from the cell. New viruses won’t be produced if the codes aren’t right—foreign proteins could be broken down prematurely, packaged incorrectly, or abandoned in situ. Humans, mosquitoes, birds, fish, turtles (and everything else) differ in cellular mechanics, and while viruses are extremely versatile and adaptable, they simply aren’t compatible with cells in every animal.
The extra-cellular environment. Blood, stomach acid, and connective tissue can be difficult for a virus to traverse. Between acidity, antibodies, and dense, impenetrable fibers, navigation throughout the body of a host can be challenging, if not deadly.
Fantastic Voyage: Mosquito Edition. Viruses must evade the immune system, enter the cells of the midgut, and replicate before migrating to the salivary glands and other body tissues. Within a vector population, there is a genetic diversity in cell receptors, encapsulation/melanotic immune responses, and permissibility to dissemination throughout tissues. Higher initial doses of viruses can overcome density-dependent responses by the mosquito, while viruses infecting younger mosquitoes are more likely to complete their development, ultimately being transmitted to other animals or humans.
Life outside of the mosquito. Viruses are affected by a number of variables, both directly and indirectly. Some viruses can survive on non-living objects for a period of time (fomites). Others may infect alternate hosts. Extrinsic higher temperatures and climatic oscillations, i.e. El Niño, can affect a virus’s ability to migrate to other tissues in a mosquito’s body, while also contributing to vector species range expansion and increased disease incidence. Overwintering is another challenge, especially in temperate climates. Viruses may remain in the tissues of hibernating adult mosquitoes during the winter, or become locally extinct, only to be reintroduced every spring by birds migrating from the tropics.
Alternate hosts. Other suitable host species can provide overwintering grounds for viruses and help maintain viral populations at very low levels in unsuspecting places. For example, the Western equine encephalitis virus, which is spread by the mosquito Culex tarsalis to horses and humans (birds are a reservoir), has also been found to infect frogs, snakes, and mosquito species feeding on cold-blooded animals. Other interesting aspects of virus–host ecology are the dilution and spillback effects of having alternate hosts present. A dilution effect occurs when alternate hosts “steal” the viral load, so other species are infected less—essentially, the same amount of virus is spread out over a larger number of hosts. Spillback effects, however, are the result of alternate hosts providing a hospitable refuge for the virus (at a cost to their own health, of course), which increases the viral population of an ecosystem.
There was an idea, way back when, that malaria transmission could be reduced via the dilution effect by introducing cattle into an ecosystem. In theory, the mosquitoes bite cattle instead of humans, but in reality the cattle didn’t have much of an effect on human biting rates (or just made things worse). In a different example, a spillback effect was observed for Buggy Creek Virus when invasive house sparrows (an alternate host) were present, resulting in increased prevalence of the virus in cliff swallows, the native host of Buggy Creek Virus.
Cultural variables. Lifestyle can limit exposure to mosquitoes; in Texas, air conditioning keeps people indoors, and there are only rare dengue outbreaks because of reduced mosquito–human interaction. Without this type of cultural control in Mexico, however, dengue occurs in epidemics. Urban environments, which can be less-than-ideal for mosquitoes, can reduce the presence of the viral population to a point where it becomes locally extinct, but sustained urban cycles of mosquito–human interactions can maintain a robust viral population.
In a long con lasting nearly 100 million years, a crafty braconid wasp stole a virus’s DNA to control the immune system of its prey.
Braconid wasps are unique parasites that lay their eggs inside unsuspecting butterfly or moth larvae, in which newly hatched wasps feed on relatively nonessential organs. Normally the immune system of the host defends against these attacks, but the wasps have a secret weapon in their arsenal: a domesticated virus from the Cretaceous period used to ensure the prey stays incapacitated but alive…until the young wasps are old enough to search out alternative food sources, that is.
The viruses coopted by braconid wasps are a type of polydnavirus (PDV), an infectious agent barely recognizable as a virus at all. Typical “everyday” viruses—like influenza or the common cold—contain all of the genetic information needed to replicate, but the genes involved in PDV reproduction are stored within the wasp’s DNA, which is an odd habit for a virus. As a result, the wasps more or less control the manufacture of the viruses and produce them at will.
Nearly 100 million years ago when the DNA coding for PDV replication was integrated into the wasp’s genome, virulence genes encoding wasp venom were transferred into the virus. Like Cold War-era microfilm, these DNA sequences contain sensitive information capable of great destruction. With these genes packaged into the shell of the stolen virus, braconid wasps literally invented nanotechnology for use in predator–prey warfare.
Think not what your virus can do for you, but what your virus can do for your baby wasps. After the mother wasp transmits the modified virus while laying its eggs, the prey’s blood cells read the DNA message inside the virus. Traditionally, this is how viruses hijack cellular machinery in order to reproduce, but after the braconid wasp’s slight-of-hand millions of years ago, the host’s cells are tricked into producing wasp venom instead of new viruses—effectively silencing the host’s own immune system so the young wasps can develop in secret.
By tricking larvae into poisoning themselves, braconid wasps save a lot of time and energy they would have otherwise used to produce their own venoms. They also gained more control over venom delivery—if the PDV integrates into a host larva’s genome, infected cells can be reprogrammed to deliver small doses of venom days or even weeks after the initial attack.
Using viruses for genetic hacking is unique among braconid wasps and several species of ichneumons, but many other wasps transmit viruses as well. Ascoviruses and baculoviruses, for example, are two types of contagion that infect butterfly and moth larvae. The parasitic wasp is only a disease vector in this case, just as mosquitoes transmit West Nile Virus to humans without infecting themselves. Ascovirus and baculovirus infections lower the immune defenses of the prey, making it easier for immature wasps to feed and grow without interference.
The relationship between wasps and viruses is symbiotic. The wasp’s young are able to develop without fear of an immune system attack and the viruses have better access to hosts. But for braconid wasps and their PDVs, the virus completely relies on the wasp for reproduction. PDVs can be selfish, though. If a caterpillar survives being parasitized by young wasps, small pieces of the virus may join with the host’s DNA to be inherited by future offspring. This is not an ideal situation for the virus, but it does remove some the virus’s reliance on the wasp for reproduction and transmission. However, these fragments of virus DNA would need to hijack DNA from another virus in order to become infectious again…but that’s just science fiction.
Or is it science fiction? In the laboratory, scientists have successfully made super-viruses from pieces of Langet and mosquito-borne dengue viruses. These and other “Frankenviruses” are typically inactive and used to create vaccines against dangerous diseases, but as for our friendly neighborhood PDVs…perhaps over the next 100 million years another insect will reengineer them in newer, even more unimaginable ways.
Herniou, Huguet, Thézé, Bézier, Periquet, & Drezen. (2013). When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviuses. Phil Trans R Soc B, 368, 20130051. doi: 10.1098/rstb.2013.0051
Gunderson–Rindal & Pedroni. (2005). Characterization and transcriptional analysis of protein tyrosine phosphatase genes and an ankyrin repeat gene of the parasitoid Glyptapanteles indiensis polydnavirus in the parasitized host. J Gen Virol, 87(2), 311–322. doi: 10.1099/vir.0.81326-0
Pletnev, Bray, Hanley, Speicher, & Elkins. (2001). Tick-borne Langat/mosquito-borne dengue flavivirus chimera, a candidate live attenuated vaccine for protection against disease caused by members of the tick-borne encephalitis virus complex: evaluation in rhesus monkeys and in mosquitoes. J Virol, 75(17), 8259–8267. doi: 10.1128/JVI.75.17.8259-8267.2001